Plant Ecology and Evolution 146 (2): 173–182, 2013
http://dx.doi.org/10.5091/plecevo.2013.816
REGULAR PAPER
Small-scale diversity of plant communities and distribution of species
niches on a copper rock outcrop in Upper Katanga, D.R.Congo
Edouard Ilunga wa Ilunga1,2,*, Maxime Séleck2, Gilles Colinet3,
Michel-Pierre Faucon4, Pierre Meerts5 & Grégory Mahy2
Université de Lubumbashi, Faculté des Sciences Agronomiques, Lubumbashi, Democratic Republic of Congo
Departement of Forest, Nature and Landscape, Biodiversity and Landscape Unit, Gembloux Agro-Bio Tech, University of Liège, 2 Passage
des Déportés, BE-5030 Gembloux, Belgium
3
Department of Science and Environmental Technology, Soil & Water Systems Unit, Gembloux Agro-Bio Tech, University of Liège, 2
Passage des Déportés, BE-5030 Gembloux, Belgium
4
HYdrISE (Hydrogeochemistry Interactions Soil Environment) unit, Institut Polytechnique LaSalle Beauvais (ISAB-IGAL), 15 rue Pierre
Waguet, FR-60026 Beauvais, France
5
Laboratory of Plant Ecology and Biogeochemistry, Université Libre de Bruxelles, 50 Avenue F. Roosevelt, BE-1150 Brussels, Belgium
*Author for correspondence: [email protected]
1
2
Background and aims – In Katanga (D.R.Congo), outcrops of bedrocks naturally enriched in Cu and
Co (“copper hills”), host unique plant communities. The spatial variation of vegetation has long been
attributed almost exclusively to variation in Cu concentration in the soil, but this assumption has not been
experimentally tested. We analysed the variation in plant communities and the niches of selected species in
relation to edaphic factors within a copper hill.
Methods – Forty-eight 1 m2 plots were sampled for plant community and soil mineral element composition,
and classified with Unweighted Pair Group Method with Arithmetic mean (UPGMA) using the Bray-Curtis
distance. Plant-edaphic relationships were examined using a Canonical Correspondence Analysis (CCA).
Species niches were modelled with Generalized Additive Model (GAM). Mean edaphic factors between
the soil of plant communities were compared with one-way Kruskal-Wallis non-parametric ANOVA.
Key results – The diversity of communities at the site scale was higher than observed in previous studies
at a larger scale. Cu was the most discriminating edaphic factor of plant communities. However, detailed
comparisons of mean edaphic factors among communities revealed individual combinations of edaphic
parameters for each community, as well as differences in soil Cu content. High covariation appears to be an
essential trait of the edaphic factor variation of Katangan Cu-rich soils. This makes it difficult to examine
separately the effect of these factors on plant community structures. A bimodal pattern of niche distribution
was found for Cu and pH. For physical parameters, niche optima were normally distributed.
Conclusions – Global variation in edaphic factors associated with variation in combinations of edaphic
parameters generates a highly heterogeneous environment favourable to a high diversity of plant
communities over limited areas. Conservation strategies or restoration actions to limit the impact of mining
activities on Cu-enriched ecosystems should pay special attention to recreate heterogeneity, taking into
account the covariation of edaphic factors.
Key words – conservation, copper, ecological niche, heavy metals, mining activities, plant community,
vegetation.
INTRODUCTION
Identification of the factors that control the distribution and
abundance of plant communities is a central problem in
ecology, which can be addressed at all spatial scales, ranging from continental scales to patchy or highly restricted mi-
crohabitats (Keddy 2007). The problem of plant community
variation is more often assessed over a large scale, encompassing obvious environmental gradients or patchy heterogeneity. However, it is clear that environments can also vary
over very small spatial scales and this small-scale variation
directly impacts on plant assemblages (Odum 1988, Vivian-
All rights reserved. © 2013 National Botanic Garden of Belgium and Royal Botanical Society of Belgium – ISSN 2032-3921
Pl. Ecol. Evol. 146 (2), 2013
Smith 1997, Grace et al. 2011). Among the factors that are
main contributors to the diversity and distribution of plant
communities, edaphic conditions are of primary importance,
whether they influence plant communities through resource
availability, water stress or toxicity stress. From all the chemical edaphic factors that might influence plant assemblages,
heavy metals have a long history of interest. Throughout the
world, metal-rich soils host highly distinctive plant communities that result from deterministic species selection by environmental filters and random processes in insular habitats
(Ernst 1974, Kruckeberg 1984, Bergmeier et al. 2009, Bes et
al. 2010, Saad et al. 2012). Due to the severe selection pressure resulting from metal toxicity, they also offer outstanding examples of microevolution and speciation processes and
very often host rare endemic taxa adapted to elevated concentrations of heavy metals (Antonovics et al. 1971, Brooks
et al. 1982, Rajakaruna 2004, Faucon et al. 2010, Harrison
& Rajakaruna 2011). Small scale variation in edaphic conditions in metalliferous sites have been demonstrated to affect
physiological and evolutionary process (Malaisse et al. 1983,
Bizoux et al. 2008, O’Dell & Rajakaruna 2011, Yost et al.
2012), species distribution (Rajakaruna 2004) and, ultimately, variation in plant assemblages (Ernst 1974, Bizoux et al.
2004, Tsiripidis et al. 2010).
Throughout the world, the flora of metalliferous soils is
threatened by human activity and actions aimed at preserving
metallophyte species are imperative (Whiting et al. 2004).
Designing conservation and rehabilitation programmes, including restoration of habitats, is urgently needed, to limit
the extinction risk of metallophyte plants and ecosystem loss
(Whiting et al. 2004, ICMM 2006). Such a strategy relies on
a sound understanding of the ecological niche of the target
species and of factors that determine plant community composition at different spatial scales (Whiting et al. 2004, Chipeng et al. 2010, Faucon et al. 2012a).
Katanga (D.R.Congo) and adjacent areas of Zambia host
one of the world’s largest concentrations of Cu-Co deposits
(Yoshida et al. 2004, Cailteux et al. 2005). Outcrops of bedrocks naturally enriched in Cu and Co, host highly original
herbaceous plant communities, which sharply contrast with
those of the surrounding forest (Duvigneaud 1958, Duvigneaud & Denaeyer-De Smet 1963). The Katangan metallicolous flora, known as the copper flora, hosts about 600
plant species tolerant to high concentrations of Cu-Co in
soils (metallophytes) (http://copperflora.org/), 32 of which
are strict endemics of metal-rich soil and 24 are broad endemics (Faucon et al. 2010). Katangan metallophytes represent an important biological resource to the D.R.Congo,
as they might serve in the ecological restoration of heavy
metal-polluted soils (Whiting et al. 2002, 2004, Faucon et
al. 2010). Due to the revival of mining activities, most Katangan copper outcrops have been allotted to mining companies (Malaisse et al. 1999, Whiting et al. 2004) and will
be irreversibly damaged in the coming decades. A number of
endemics have already become extinct (Faucon et al. 2010,
Faucon et al. 2012b).
Pioneering studies on these ecosystems, based on a classical phytosociological approach (Duvigneaud 1958, Duvigneaud & Denaeyer-De Smet 1963, Malaisse et al. 1994),
revealed the existence of patterns of vegetation on copper
174
hills, with characteristic zonation along the slopes. Plant
communities for each outcrop were organised along steep Cu
gradients related to the outcrop topography (Duvigneaud &
Denaeyer-De Smet 1963). However, plant communities described by physiognomic criteria did not provide a fine scale
understanding of plant community diversity in relation to
edaphic factors. Recent studies, based on modern sampling
methods, support the idea that other soil factors, especially
pH, Mn-oxides, Fe-oxides and organic matter should also be
considered (Kabala & Singh 2001, Neaman et al. 2009, Faucon et al. 2011a). Interaction with metals other than Cu and
Co might also limit their bioavailability and thus soil toxicity. Saad et al. (2012) suggested that nutrient status might
also be of prime importance. To date, no detailed studies
have focused on an assessment of the diversity of Cu plant
communities in relation to edaphic factors at a small scale.
Patchiness of metalliferous habitat might lead to high beta
(inter-site) diversity for flora (Harrison & Inouye 2002, Harrison & Rajakaruna 2011), thus obscuring intra-site variation
in large-scale studies. Examining the small-scale diversity of
plant communities within single Cu sites is particularly important, to assess the effort that should be devoted to restoration strategies.
Apart from plant assemblages, single species belonging
to similar plant communities are expected to react differently
to the combination of environmental groupings. Understanding the individual niche of metallophyte species as well as
the niche distribution along environmental gradients is essential for a fine-tuning of species conservation strategies in
restored habitats (Bizoux et al. 2004, Chipeng et al. 2010,
Faucon et al. 2011b). The ecological niches of only a few
species growing on Cu outcrops have been characterised:
Ocimum centrali-africanum (Howard-Williams 1970), Haumaniastrum katangense (Malaisse & Brooks 1982, Paton &
Brooks 1996, Chipeng et al. 2010), Mimulus cupriphilus, M.
guttatus (Macnair & Gardner 1998), Crepidorhopalon perennis and C. tenuis (Faucon et al. 2012b).
In this study, we address the degree to which small-scale
continuous edaphic gradients can contribute to plant assemblage diversity and the consequences for restoration of metallophyte vegetation. The specific objectives of this study
were to: (1) analyse the pattern of fine-scale plant community variation within a Cu site subject to a strong ecological
gradient; (2) assess the distribution of ecological niches for
a set of species representative of those communities for conservation and restoration purposes, and (3) compare our results with those of other studies performed on a larger scale,
to infer implications for plant communities and species conservation at the small scale.
MATERIALS AND METHODS
Site description
Kinsevere outcrop is located at 11°36’S 27°58’E in the eastern part of the Katangan Copper Belt, 30 km north-north-east
of Lubumbashi, D.R.Congo. The outcrop (surface approximately 9 ha, hill height around 25 m) is covered by swards
on a plateau (1,263 m) with a gentle slope and flat area (contamination dembo) at the base of the outcrop, both character-
Ilunga wa Ilunga et al., Species niches on a copper rock outcrop in Upper Katanga, D.R.Congo
ized by steppic savannas. The copper hill is surrounded by
miombo woodland with Brachystegia spp. Swards occur on
reworked mine debris and consist of open vegetation mainly
composed of annual species, long-lived short grasses and dicotyledonous species not exceeding 40 cm in height. Steppe
savannas consist of dense vegetation on primary habitats
dominated by long-lived tall grasses and dicotyledons with
woody underground systems not exceeding 80 cm in height.
The climate is subtropical humid, CW6s according to
the Köppen classification (Bultot 1950). There is one rainy
season (November to March) and one dry season (May to
September), with two transition months (October and April).
Mean total annual rainfall is 1.273 mm of which 1.122 mm
falls during the rainy season (Anvil Mining Compagny Katanga, unpubl. data). Mean annual temperature is 21°C. The
temperature is the lowest at the beginning of the dry season
(15–17°C). September and October are usually the warmest
months with daily maxima of 31–33°C. The rainy season is
characterised by the flowering of grasses and the dry season,
by flowering of geophyte species stimulated by wildfires.
Soil sampling and vegetation cover estimation
Vegetation was sampled along two parallel transects (230 m
in length) placed north-east to south-west along the main
slopes. The transects were 25 m apart and encompassed the
entire physiognomic variation of the outcrop’s vegetation related to the topographic gradient. Forty eight permanent 1m2
plots were located at 10 m interval along the transects.
To characterise plant communities, all plant species were
recorded in each plot on four dates, corresponding to the
phenological variation of Katangan vegetation: August 2008
(end of dry season), December 2008 (first part of wet season), February 2009 (mid wet season) and April 2009 (beginning of dry season). Species abundances were recorded using the Braun-Blanquet scale: +: < 1% cover, 1: 2–5% cover,
2: 6–25% cover, 3: 26–50% cover, 4: 51–75% cover and 5:
76–100% cover (Poore 1955). Nomenclature was based on
the Flora Zambesiaca (Board of Trustees Kew Royal Botanic Gardens 1960–2010) and the Flore d’Afrique Centrale
(Bamps 1973–1993). Authors of taxa and families to which
they belong are given in the electronic appendix 1.
Plant collections were deposited at the herbaria of the
Faculty of Agronomy (University of Lubumbashi) and the
Biodiversity and Landscape Unit (Gembloux, Belgium).
Composite soil samples (200 g) were collected in December
2008 in the upper soil layer (0–40 cm) of each plot. Each
sample consisted of a bulk of five samples collected in the
centre and the four corners of the 1 m2 plot. Soil samples
were air-dried and sieved to 2 mm and the percentage of
stones (> 2 mm) was measured. The pH was measured in water or in 1N KCl with a glass electrode in a 2:5 soil:solution
ratio and with 2h equilibration time. Total organic content
was measured following the Springer-Klee method (Springer
& Klee 1954), via hot oxidation with K2Cr2O7 and titration of
the excess oxidant with (NH4)2Fe(SO4)26H2O. Total nitrogen
was determined following the Kjeldahl method (Bremner
& Mulvaney 1982). The bioavailability of Cu, Co, Zn, Fe,
Mn, K, Mg, Ca and P were determined after an extraction by
1N CH3COONH4EDTA (pH 4.65) for 30 min (ratio
soil:solution of 1:5) (Lakanen & Erviö 1971). The supernatant was filtered through a S&S 595 folded filter and analysed
using a flame atomic absorption spectrometer (Varian 220).
Phosphorus content was determined with a Shimadzu UV1205 spectrophotometer (Shimadzu Corporation) at 430 nm
after the development of blue colouration.
Identification of plant communities
Prior to statistical analysis, Braun-Blanquet coefficients were
transformed into ordinal van der Maarel values: 1, 3, 5, 7, 8
and 9 (van der Maarel 2005). All seasonal relevés were compiled, selecting the highest abundance of each species in a
plot. This method allows the phenological variation of flora
in Katanga to be taken into account (Saad et al. 2012). Plant
communities were identified through a hierarchical UPGMA
classification using the Bray-Curtis distance (Dufrêne &
Legendre 1997). The resulting hierarchical tree was analysed
to define the main plant communities at 80% similarity. The
80% similarity criterion was selected, to allow comparison
of results to those of recent studies (Saad et al. 2012). Indicator species for each plant community were identified with the
IndVal method (Dufrêne & Legendre 1997). To examine the
relationships between floristic data and the different edaphic
variables, a Canonical Correspondence Analysis (CCA) was
performed. Finally, one-way Kruskal-Wallis non-parametric ANOVA followed by Tukey’s HSD test was performed
to test differences between environmental variables among
plant communities identified with the hierarchical classification (Oksanen 2010). Because edaphic parameters might
covary along environmental gradients, we first explored the
structure of edaphic factor variation at the study site via Principal Component Analysis (PCA).
Species ecological amplitude
The distribution of ecological niches along edaphic factors
was explored for twelve species present in at least ten plots:
Andropogon schirensis, Bulbostylis pseudoperennis, Cryptosepalum maraviense, Digitaria nitens, Eragrostis racemosa, Gladiolus tshombeanus, Hibiscus rhodanthus, Loudetia
simplex, Monocymbium ceresiiforme, Ocimum centrali-africanum, Scleria sp. and Tristachya bequaertii. Generalised
additive models (GAM; Hastie & Tibshirani 1990) – a nonparametric extension of generalised linear models (GLM) –
with binomial likelihoods were used to model the probability
of species abundance in relation to edaphic parameter values
(Lepš & Šmilauer 1999) using CANOCO version 4.5 (ter
Braak & Šmilauer 2002).
In a first step, each edaphic parameter pH water, pH KCl,
Cu, Co, C, N, P, Cd, Zn, Fe, Mg, K, Pb, Mn, Ca, % rock
cover, % stones in soil, slope) was separately tested against
the twelve species. Only edaphic parameters for which at
least half of the species had a significant GAM model (P <
0.01) were retained. To select the main factors potentially affecting species ecological niches at the studied site, we retained edaphic factors that best explained the abundance of
the twelve selected species in a Canonical Correspondence
Analysis (CCA). For each of the retained combinations,
species-edaphic parameters, and the optimum and central
border of the niche amplitude were estimated. The central
175
Pl. Ecol. Evol. 146 (2), 2013
border is equivalent to the classical estimation of tolerance
for the Gaussian response curve (Heegaard 2002, Heikkinen
& Mäkipää 2010).
The fraction defining the central borders was computed
following the formula: c×exp(-2); with (c) as the maximum
response (Heegaard 2002).
RESULTS
Edaphic factor variation
Variation among plant communities is the result of geochemical contamination primarily by Cu, possibly associated with
Ca, Zn, Pb, Cd and to a lesser degree, the effect of organic
matter. The first two axes of the PCA for eighteen edaphic
variables explained 50% of the total variation (fig. 1). The
variables that best correlated with PCA1 were Cu, pH KCl,
N, C, Zn, Cd, Ca, Pb and P (positive correlation) and the
variables best correlated with PCA2 were % rock cover,%
stones in soil and Co (positive correlation) and K, Fe and
Mg (negative correlation). On the second axis, without relation to the first axis, a greater % rock cover on the surface
was associated with a greater % stones in soil and the poorest correlation was the habitat i.e. deficiencies in Mg, Fe and
K (fig. 1). Altogether, the analysis suggests intercorrelation
among numerous edaphic variables. Four main groups of parameters were identified: Cu-pH KCl-P, N-C-Zn-Cd, % rock
cover-% stones in soil-Co, this latest opposed to Mg-Fe-K.
Plant communities
A total of 64 species were identified in the 48 plots. Five
groups of plots were identified from the hierarchical classification at 80% similarity, and were interpreted as five different plant communities (fig. 2A & B). Each community was
well characterized by a set of indicator species (fig. 2A & B).
Communities I and III corresponded to swards and steppe
savanna, respectively, supplied with malachite gravel from
the outcrop plateau. An indicator species for community I
was Haumaniastrum katangense, an annual species. Community II corresponded to sward developing mainly on the
plateau with a high proportion of malachite. Indicator species for community II were three short-stature perennial
species with low rooting-depth systems: Lapeirousia ery­
thrantha, Ipomoea linosepala subsp. linosepala and Bulbostylis pseudoperennis. Community III was characterised by
Commelina sp., Bulbostylis filamentosa a short hemicryptophyte, and Vernonia suprafastigiata, a species developing a
deep underground xylopode. Communities IV and V were
typical steppe savannas located on different parts of the topographical gradient: the outcrop foot for community IV and
dembo for community V. Community IV was characterised
by Tri­stachya bequaertii and Digitaria nitens, two clonal
gramineae, and Cryptosepalum maraviense, a soil-covering
sub-shrub with well-developed underground xylopodes.
Community V was also dominated by gramineous species;
its indicator species were three sub-shrubs with well-developed underground xylopodes: Eriosema englerianum, Hibiscus rhodanthus and Ocimum centrali-africanum (fig. 2A &
B).
Plant communities and edaphic factors
Figure 1 – Principal Component Analysis of 18 edaphic factors in
48, 1 m² plots on the Kinsevere copper outcrop. Arrows represent
edaphic factors.
176
Five groups of relevés identified in the clustering analysis
were distinguished well in the CCA analysis. The first two
axes of the CCA explained 37% of the total variation. The
first axis clearly opposed Communities I, II and III (positive
values) to communities IV and V (negative values) and was
positively correlated with trace metals and C-N content and
negatively correlated with Mg, K and Fe.
Community II was also distinct from community I and
III along axis 1 but the two latter communities were less distinguished. Axis 2 clearly separated communities IV and V,
with negative coordinates for community IV being correlated
mainly with slope, % of stones in soils and Fe.
There were differences in mean edaphic variables among
the three communities for 12 of the 20 variables tested (table 1). Due to the number of tests and the intercorrelation
of edaphic variables (table 1), associated probabilities should
be taken with caution. However, careful examination of intercommunity differences highlights the complex nature of
relationships among plant communities and edaphic parameters.
Cu was the best discriminating factor among communities (F4,34 = 52.74) and clearly distinguished communities
I and III from community II with a high mean Cu content
(1,131–12,874 mg/kg) and community IV from community
V with a lower mean Cu soil content (111–289 mg/kg). The
soil of community II not only exhibited the highest level of
Ilunga wa Ilunga et al., Species niches on a copper rock outcrop in Upper Katanga, D.R.Congo
A
B
Figure 2 – Identification of plant communities, indicator species and relationships with edaphic parameters on the Kinsevere copper outcrop,
Katanga, D.R.Congo. A, dendrogram generated from an UPGMA analysis performed on the Bray-Curtis distance similarity of species composition in 1 m² plots. Indicator species are shown with their IndVal value in brackets. B, canonical correspondence analysis (CCA) based on
species composition and 18 environmental parameters in 48, 1 m² plots. The first two axes of the CCA explained 37% of the total variation.
Table 1 – Mean and standard errors of edaphic factors for the partitions in five communities identified at the Kinsevere copper
outcrop.
*Significant differences in mean edaphic factors among groups after Bonferonni adjustment: P < 0.003. (Bonferonni adjustment: P value =
0.05/n variables); Superscript letters (a,b,c,d) indicate homogeneous groups (Tukey’s HSD test, Kruskal Wallis non parametric ANOVA); n =
number of samples per group. F4,34 = Fischer significance test at 4 and 34 degree of freedom.
Environment variables
pHwater
pHKCl
C (g/100)
N (g/100)
Cu (mg/kg)
Co (mg/kg)
Zn (mg/kg
Cd (mg/kg)
Pb (mg/kg)
Ca (mg/kg)
Mg (mg/kg)
K (mg/kg)
Mn (mg/kg)
Fe (mg/kg)
P (mg/kg)
Slope (°)
Stones in soil (%)
Rocks cover (%)
Group
1 (n = 7)
2 (n = 10)
3 (n = 7)
4 (n = 10)
5 (n = 5)
F4,34
5.2 (0.4)a
4.4 (0.3)a
1.7 (0.7)a
0.13 (0.05)a
1131 (1149)c
6.6 (6.5)a
0.97 (0.7)a
0.03 (0.03)a
1.64 (0.89)a
77 (72)a
79 (31)a,b
76 (44)a,b
49 (44)a
65 (32)a
143 (237)a
11 (12)a,b
52 (6)c
77 (37)c
5.5 (0.3)a
4.8 (0.2)b
6.1 (1.5)c
0.44 (0.09)c
12874 (6099)d
3.2 (4.1)a
4.89 (2.77)b
0.18 (0.09)c
2.77 (2.4)a
176 (149)a
57 (32)a
67 (46)a
31 (39)a
43 (21)a
213 (86)b
13 (7)b
42 (11)b,c
51 (32)b,c
5.4 (0.2)a
4.3 (0.2)a
4.3 (1.6)b
0.3 (0.12)c
1854 (1780)c
3.4 (4.3)a
2.34 (1.93)a,b
0.11 (0.07)b,c
3.37 (2.54)a
151 (108)a
138 (48)b,c
110 (57)a,b
48 (31)a
115 (32)b
67 (43)a
13 (9)b
30 (10)a,b
13 (16)a,b
5.5 (0.2)a
4.3 (0.3)a
2.9 (0.5)b
0.19 (0.02)b
289 (84)b
2.6 (2.2)a
1.58 (0.79)a
0.07 (0.02)b
2.29 (0.79)a
124 (99)a
196 (89)c
143 (48)b
54 (32)a
135 (34)b
83 (136)a
12 (5)b
29 (10)b
8 (7)a
5.4 (0.2)a
4.2 (0.1)a
2.1 (0.3)a
0.15 (0.02)a
111 (52)a
2.5 (1.1)a
0.96 (0.23)a
0.03 (0.02)a
2.26 (0.23)a
87 (63)a
81 (36)a,b
101 (66)a,b
24 (10)a
60 (9)a
27 (5)a
0 (0)a
17 (6)a
0 (0)a
0.54
6.77*
35.89*
29.66*
52.74*
0.58
9.14*
15.22*
0.76
1.35
12.93*
4.2
2.01
15.73*
8.44*
4.34*
14.01*
10.7*
177
Pl. Ecol. Evol. 146 (2), 2013
Cu but was also distinguished from other communities by
higher levels of C and P. The soil of community I, while exhibiting very similar levels of Cu to community III, was distinguished by lower levels of C and N.
Communities III and IV, while very different in Cu content, were both distinguishable from other communities by
higher levels of Fe and, in part, Mg. The physical structure of
the soil was also different among communities with soils of
community IV and V, exhibiting a lower % stones in soil and
lower % rock cover as compared to community I. Communities II and III showed intermediate mean values for these
parameters.
Species ecological niches
For thirteen out of the eighteen edaphic variables, at least six
species displayed a significant GAM model: % rock cover
(n = 12); Cu (n = 10); pH KCl (n = 10); C (n = 9); N (n = 9);
P (n = 9); Cd (n = 9); Zn (n = 8); Fe (n = 7); Mg (n = 7); K
(n = 7); Pb (n = 7); % stones in soil (n = 6).
From these edaphic parameters, % rock cover, Cu, pH
KCl and % stones in soil were the most prominent in ex-
plaining the variation in abundance of the twelve species in
relation to edaphic factors based on a CCA analysis for these
twelve species (not shown). Repartition of the niche optimum along the environmental gradients was different among
the chemical and physical soil parameters (fig. 3). For Cu,
ten species were situated with no niche optimum within the
intermediate value, irrespective of the value of the gradient.
The superimposition of ecological niches for Cu content was
due to differences in niche amplitude among species with the
highest optimum, also exhibiting the largest niche. A similar
bimodal pattern was found for pH KCl. In contrast, niche optima were distributed normally along the gradient for physical parameters (% rock cover and % stones in soil), but a
tendency to increase in niche amplitude with an increase in
optimum values was also observed.
DISCUSSION
Pattern of fine scale plant community variation within a Cu
site subjected to a strong ecological gradient
A small-scale gradient of environmental conditions is
important to evolutionary processes, species coexistence and
A
C
B
D
Figure 3 – Estimation of species ecological responses along environmental gradients with the optimum (black dot) and central borders (grey
line). A, Cu; B, % rock cover; C, pH KCl; D, % stones in soil.
178
Ilunga wa Ilunga et al., Species niches on a copper rock outcrop in Upper Katanga, D.R.Congo
ultimately to the diversity of plant assemblages (Silvertown
2004). In this study, we found complex variation of edaphic
conditions within a single metalliferous site. Such a complex
pattern of edaphic variation is generated by a high covariation among edaphic factors. Small-scale edaphic variation
within a single Cu site appeared as large as the variation
demonstrated for combinations of Cu sites over a large spatial scale in both physical (stones in soil, rock cover) and
chemical factors (Cu, Fe, Mg, P, K, N, C, and Zn) (Faucon et
al. 2011b, 2012b, Saad et al. 2012). This variation in edaphic
factors generates a highly heterogeneous environment, promoting niche diversity and therefore inducing a high diversity of plant assemblage over limited areas. The diversity of
plant communities (N = 5) identified in our study site was
higher than that (N = 3) identified by Saad et al. (2012) over
six isolated Cu outcrops at a sub-regional scale based on the
same criteria of analyzing plant-edaphic relationships.
This high local diversity of plant communities might be
interpreted with respect to different combinations of edaphic
conditions, in agreement with most recent studies on Cu vegetation (Faucon et al. 2011b, Saad et al. 2012). Obviously,
due to its large variation, Cu concentration is the most discriminant edaphic factor among identified plant communities. However, not only variation in the concentration of Cu
might be determinant for the structuration of plant diversity
on Cu outcrops: analysis of covariation among floristic data
and edaphic data (CCA) indicated a correlation of numerous
edaphic factors with floristic variation.
Detailed comparisons of mean edaphic factors among
communities also revealed individual combinations of
edaphic parameters for each community apart from differences in soil Cu content. Nevertheless, correlations among
edaphic factors should be taken with caution, given differences in soil properties due to horizon depth differences between habitats. Communities with a high level of soil Cu (I,
II, III) also differed in other parameters including nutrients.
Metallicolous communities associated with higher nutrient
concentrations than other communities, differ from those on
serpentine soils, where deficiency of N, P, K and Ca has been
suggested as a potential reason for limited plant productivity
(Kruckeberg 1984, O’Dell et al. 2006). Communities with a
lower Cu contamination (IV, V) also differed from each other
notably in Fe and Mg. Heavy metals are antagonistic to the
uptake of other elements (Kazakou et al. 2008) and high values of Fe-oxides can limit Cu availability and thus its toxicity
at low contamination levels (Kabala & Singh 2001). Furthermore, Fe is known to have antagonist effects on Cu uptake
(Faucon et al. 2009). The large variation in physical properties of soil observed in our study should also play a role in
filtering the assemblage of plants on Cu-rich soil. This might
promote specific local conditions, such as reworked substrate
typical of community I, where the therophytic pioneer species Haumaniastrum katangense dominates (Faucon et al.
2011b). Interestingly, Saad et al. (2012) found similar patterns of covariation in a multi-site study situated in another
Katangan region (Tenke), with strong correlations within the
same groups of edaphic factors: N-C and Fe-Mg-K. Covariation was shown by C and N, which is possibly explained by
a high Cu content reducing mineralisation speed. The negative correlation between % stones in soil-rock cover and Mg-
Fe-K might be explained by dilution of fine soil particles by
quartz or by the presence of clayey rocks on the slope. High
covariation appears to be an essential trait of edaphic factor
variation of Katangan Cu-rich soils. This will make it difficult to examine separately the effect of these factors on plant
community structures.
The plant communities identified in our study based on
modern quantitative methods match closely the vegetation
units identified via physiognomic criteria or traditional phytosociological approaches in pioneer studies (Duvigneaud
1958, Duvigneaud & Denaeyer-De Smet 1963). The first
partition of the hierarchical clustering establishes the wellknown distinction between low mineralized steppic savannas and highly contaminated swards. Individual communities might also be linked to previously described vegetation
units: community I and III = swards with annual polycuprophytes on disturbed soil; community II = sward/steppe with
polycuprophytes; community IV = steppic savanna on slope;
community V = dembo steppic savanna.
Distribution of ecological species niches in heterogeneous
environment
The concept of the ecological niche holds a central role in
ecology as it has been widely used to understand species coexistence within communities and to predict species distribution along environmental gradients (Violle & Jiang 2009).
Wide variation in edaphic factors might also be expected
to promote a diversity of ecological niches for individual species. Niche distribution along edaphic gradients has not been
previously examined for species growing on Cu outcrops.
Our results showed two different patterns for soil chemical
and physical parameters. Niche optimum distribution was
clearly bimodal for chemical factors, particularly for Cu.
However, a high proportion of species with a niche optimum
at the lowest Cu concentrations might partly be due to the
fact that 67% of quadrats contained fewer than 1,000 ppm
of soil Cu. In contrast, the distribution of the niche optimum
was more regular along the gradient of physical parameters.
Examination of niche amplitude also generates interesting hypotheses concerning the evolution of tolerance along
edaphic gradients (Baack et al. 2006). For Cu, species with
a niche optimum at higher concentrations displayed larger
amplitudes and probably greater tolerance, than species with
a niche optimum at lower concentrations. A similar pattern
was observed for physical parameters (rock cover and stones
in soil). These patterns should be interpreted with caution,
due to the low number of species examined, but might suggest new hypotheses to be further tested in a larger context.
Fine-scaled ecological heterogeneity conditions probably play important roles in niche distribution. Some situations might cause divergent selection in the population and
thus contribute to ecotypic differentiation (Antonovics et al.
1987, Bischoff et al. 2006).
In this study, the Ocimum centrali-africanum niche optimum, was limited only to soils with a lower Cu concentration
compared to that in Howard-Williams (1970, 1971), where it
was reported to vary in different soil types. This might be
partly explained by constrained physical factors associated
with the metal-rich soil of Katanga, namely % rock cover.
179
Pl. Ecol. Evol. 146 (2), 2013
Ecological restoration, a challenge due to significant
small-scale variation of plant assemblages
Our study demonstrated a high degree of small-scale diversity in plant communities (n = 5) along a Cu gradient in combination with several other edaphic factors. This is complementary to the lower diversity of plant communities found
by Saad et al. (2012) at a regional scale. Hence, our results
suggest the importance of further examination of Cu plant
community diversity in a hierarchical spatial framework, if
relevant conservation programmes have to be designed. Our
results also indicate that maintaining the diversity of plant
assemblages in post-mining rehabilitation programmes
might be challenging, due to significant small-scale variation
within those plant assemblages. With regard to restoration,
actions to be promoted to limit the impact of mining activities on those ecosystems should pay special attention to the
recreation of heterogeneous and specific conditions similar
to those of plant communities (Pope et al. 2010, Lazarus et
al. 2011). However, full restoration after re-establishing historic soil conditions will be achieved by avoiding changes
in soil conditions, such as nutrient pollution, which alleviate
edaphic stress (O’Dell & Classen 2011).
The largest amplitude of niches with an optimum in the
most severe conditions (high Cu content; rocky substrates),
suggests the possibility for those species to be maintained in
alternative habitats, for example, in secondary habitats created by mining activities, given the intensity of natural habitat
destruction. Such a situation was described by Faucon et al.
(2011b) for a Cu metallophyte but needs to be tested further
for other metallophytes in natural habitats and species with a
phytoremediation potential.
SUPPLEMENTARY DATA
Supplementary data are available in pf format at Plant Ecology and Evolution, Supplementary Data Site (http://www.
ingentaconnect.com/content/botbel/plecevo/supp-data), and
consists of a list of plant species sampled at the Kinsevere
copper hill (Katanga, D.R.Congo)
ACKNOWLEDGEMENTS
The Coopération universitaire au Développement (CUD) is
acknowledged for the financial support of this study (PIC
REMEDLU). This work is part of the research project
2.4.582.09F funded by the FRS-FNRS ERASMUS programme B. LIEGE 01 and F. BEAUVAIS 02. We are grateful to MMG Kinsevere (formerly AMCK Kinsevere Mine
project) for logistic support during field investigations, particularly to Johnnie Ntukula and Hugues Munung for their
assistance.
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